A small RNA-guided PRC2 complex eliminates DNA as an extreme form of transposon silencing

Cell Rep. 2022 Aug 23;40(8):111263. doi: 10.1016/j.celrep.2022.111263.

Abstract

In animal germlines, transposons are silenced at the transcriptional or post-transcriptional level to prevent deleterious expression. Ciliates employ a more direct approach by physically eliminating transposons from their soma, utilizing piRNAs to recognize transposons and imprecisely excise them. Ancient, mutated transposons often do not require piRNAs and are precisely eliminated. Here, we characterize the Polycomb Repressive Complex 2 (PRC2) in Paramecium and demonstrate its involvement in the removal of transposons and transposon-derived DNA. Our results reveal a striking difference between the elimination of new and ancient transposons at the chromatin level and show that the complex may be guided by Piwi-bound small RNAs (sRNAs). We propose that imprecise elimination in ciliates originates from an ancient transposon silencing mechanism, much like in plants and metazoans, through sRNAs, repressive methylation marks, and heterochromatin formation. However, it is taken a step further by eliminating DNA as an extreme form of transposon silencing.

Keywords: CP: Molecular biology; DNA elimination; H3K27me3; H3K9me3; PRC; Piwi; ciliates; heterochromatin; piRNA; transposable elements; transposons.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Argonaute Proteins / genetics
  • Argonaute Proteins / metabolism
  • DNA / metabolism
  • DNA Transposable Elements / genetics
  • Drosophila Proteins* / metabolism
  • Drosophila melanogaster* / metabolism
  • Gene Silencing
  • Polycomb Repressive Complex 2 / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism

Substances

  • Argonaute Proteins
  • DNA Transposable Elements
  • Drosophila Proteins
  • RNA, Small Interfering
  • DNA
  • Polycomb Repressive Complex 2